Discrete genetic modules underlie divergent reproductive strategies in three-spined stickleback

A central challenge in biology is to understand how complex behaviors
evolve. Reproductive behaviors are frequently subject to strong selection
and complex behavioral traits often evolve as an integrated package.
However, it is unclear whether suites of traits evolve through a few
pleiotropic genetic changes, each affecting many behaviors, or by
accumulating several changes that, when combined, give rise to an entire
package of correlated traits. Typically, three-spined stickleback exhibit
paternal care, a behavior that characterizes the entire Gasterosteidae
family. However, an unusual “white” three-spined stickleback ecotype
exhibits a suite of traits associated with the evolutionary loss of
paternal care. In the white ecotype, males disperse embryos from their
nests rather than care for them, build loose nests, exhibit high rates of
courtship, and are relatively small in body size. These differences are
apparent in stickleback reared in a common garden environment, suggesting
the differences have a heritable basis. In an F2 intercross (n=76-133), we
show that these traits are genetically uncorrelated and map to different
genomic regions, suggesting that components of the white reproductive
strategy segregate independently and evolved through the addition of
multiple genetic changes. Moreover, distinct sets of genes may be involved
in regulating the same motor pattern across contexts. These results
contribute to the growing body of evidence that behavioral diversity
observed in nature may evolve by accumulating and combining alleles, each
with modular effects, and show that this principle applies to a suite of
behavioral traits that form an integrated strategy.